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Sedimented Chemosynthetic Ecosystems of the Southern Ocean

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Sedimented Chemosynthetic Ecosystems of the Southern Ocean Sedimented Chemosynthetic Ecosystems of the Southern Ocean James Benjamin Bell Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Faculty of Earth and Environment School of Geography April 2017 i The candidate confirms that the work submitted is his own, except where work which has formed part of jointly authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. The work in Chapter 3 of the thesis has appeared in publication as follows: Geochemistry, faunal composition and trophic structure in reducing sediments on the southwest South Georgia margin. Royal Society Open Science (2016) 3; 160284. James B. Bell, Alfred Aquilina, Clare Woulds, Adrian G. Glover, Crispin T. S. Little, William D. K. Reid, Laura E. Hepburn, Jason Newton & Rachel A. Mills Contributions: JBB was responsible for the literature review; geochemical, taxonomic and isotopic analyses; statistical methods; preparation of plots and figures and for preparing all drafts of the manuscript. AA, CW, AGG, WDKR, LEH and RAM were responsible for collection of samples at sea. Additional geochemical data were collected and analysed by AA, LEH and RAM. JBB was assisted in taxonomic analyses by AGG and CTSL and in elemental and isotopic analyses by CTSL, CW and JN. All authors commented on various draft manuscripts and approved the final version. This manuscript was reviewed by Prof. David Pond (Scottish Association for Marine Science) and Prof. Lisa Levin (Scripps Institute of Oceanography). The work in Chapter 4 of the thesis has appeared in publication as follows: Macrofaunal ecology of sedimented hydrothermal vents in the Bransfield Strait, Antarctica. Frontiers in Marine Science (2016) 3: 32. 10.3389/fmars.2016.00032. James B. Bell, Clare Woulds, Lee E. Brown, Christopher J. Sweeting, William D. K. Reid, Crispin T. S. Little, and Adrian G. Glover Contributions: JBB was responsible for the literature review; taxonomic data collection; taxonomic and geochemical data analyses; preparation of figures and all drafts of the manuscript. AGG, CW, WDKR and CJS were responsible for ii collection of samples at sea. JBB was assisted in taxonomic analyses by CTSL and AGG and in statistical analyses by CW and LEB. All authors commented on various draft manuscripts and approved the final version. This manuscript was reviewed by Dr Americo Montiel (University of Magallanes, Chile) and Dr Daniella Zeppilli (French Research Institute for Exploitation of the Sea). The work in Chapter 5 of the thesis under review at the time of submitting this thesis, following an invitation from the Associate Editor to submit a revised version. Manuscript first submitted on the 27th of July 2016. Associate Editor decision 7th December 2016. Revised manuscript submitted 20th December 2016. Hydrothermal activity lowers trophic diversity in Antarctic sedimented hydrothermal vents. Biogeosciences (In review) James B. Bell, William D. K. Reid, David A. Pearce, Adrian G. Glover, Christopher J. Sweeting, Jason Newton, & Clare Woulds Contributions: JBB was responsible for the literature review; preparation of isotope samples; analysis of isotopic data; statistical methods; preparation of figures and all drafts of the manuscript. WDKR, DAP, AGG, CJS and CW were responsible for collection of samples at sea. DAP was responsible for 16S sequencing and interpretation of sediment microbial assemblages. JBB was assisted in isotopic data collection by JN and isotopic data analyses by WDKR and CW. All authors commented on various draft manuscripts and approved the final version. The work presented in Chapter 6 of the thesis was under initial review at the time of submitting this thesis. Hydrothermal activity, functional diversity and chemoautotrophy are major drivers of seafloor carbon cycling. Scientific Reports (In review) James B. Bell, Clare Woulds & Dick van Oevelen. Contributions: JBB was responsible for the literature review; collation of data; designing and implementing model code; statistical methods; preparation of iii figures and all drafts of the manuscript. JBB was assisted in model design; implementation and statistical methods by DvO and in data collation by DvO and CW. All authors commented on various draft manuscripts and approved the final version. Thesis by Alternative Format (TAF) Rationale As a consequence of the samples having being collected prior to the commencement of the studentship, primary data collection began shortly following the studentship start date. The student was then able to begin preparing manuscripts within one year of starting and the first article submission was accepted in February 2016 (Chapter 4). Subsequent submissions of the second and third data chapters were made in 2016, with chapter 3 accepted in August 2016 and chapter 5 resubmitted in December 2016, following initial reviews. Chapter 6 was in review at the time of submission. This meant that TAF was considered to be the most appropriate option for the thesis and the data chapters are organised with respect to submitted versions of each of the publications (either accepted or in review). Copies (PDFs) of each of the published manuscripts accompany this thesis as well as each having gold open access at their respective journals. Supplementary material is included as appendices on the attached CD. The student has also contributed to several other publications during the studentship, but only publications lead authored by the student that are relevant to this project are given in the thesis below. Copyright Declaration This copy has been supplied on the understanding that it is copyright material and that no quotation from this thesis may be published without proper acknowledgement. The right of James Benjamin Bell to be identified as the author of this work has been asserted by him in accordance with the Copyright, Designs and Patents Act 1988. iv 2016 James B. Bell, The Natural History Museum and The University of Leeds Acknowledgements I am enormously grateful to several people, whose support has been invaluable to me during the last three and a half years. My supervisors; Clare Woulds, Adrian Glover and Lee Brown have supported me throughout my academic development and I have particularly appreciated the repeated opportunities for self-direction and professional development. I have found the project very fulfilling and certainly hope that this won’t be the last contribution I make to marine science. Further to my two main supervisors, I’d also like to thank the numerous other people whom I’ve been fortunate enough to work with during the course of my PhD: Will Reid; Cris Little; Jason Newton; Karen Bacon; Laura Hepburn; Alfred Aquilina and Rachel Mills. Thanks also to the generous support of my examiners, Andrew Sweetman and Graeme Swindles. In particular, I’d also like to accord special thanks to Dan Jones and Claudia Alt, whose tireless support at the start of my academic career gave me the chance to get started on all this science business. I would also like to gratefully acknowledge the funding support I have received from NERC and the Natural History Museum. I would also like to thank my lovely wife, Becci, and my two wonderful daughters, Sophie and Emma for reminding me about the other important things in life, and forcing me to have a work-life balance from time to time. Thank you also to my parents, Nick and Alison, who have helped give me the opportunities to be able to have reached this stage. Even more thanks (in no particular order) to the great friends who’ve helped me on my way: Jess; Alice; Will; Joe; Owen; Scott; Liz; Sarah (F and L); Freddie; Greta; Fernanda; Adriane; Michelle and Annie. The completion of this thesis represents a major step in my life’s ambition to study the biological wonders of the deep ocean. From the age of six, I had already resolved to become a marine biologist and I am proud to able to say that I have accomplished that and incredibly appreciative of those mentioned above who have helped make it happen. v I have published papers and given talks on deep-sea biology, completed a PhD thesis in deep-sea biology, participated in a deep-sea research cruise and even done stand-up comedy about deep-sea biology. I am a deep-sea biologist. *High fives six-year old self* vi Abstract Sedimented chemosynthetic ecosystems (SCEs) are complex seafloor environments that combine several potential sources of organic matter. Their physical similarity to the vast soft-sediment habitats on the seafloor means that they can be inhabited by a diverse range of more ubiquitous fauna. This is in stark contrast to ecosystems such as hard substratum hydrothermal vents, which are typically almost totally dominated by a few specialist species. Another characteristic of these ecosystems is that they exhibit diffuse environmental gradients, relating to chemosynthetic production potential and environmental toxicity. Consequently, it is often difficult to determine their spatial extent, and the ecological responses along such gradients. A central theme of the research presented in this thesis has been to determine the role of habitat-structuring processes at two contrasting SCEs in the Atlantic sector of the Southern Ocean. I demonstrate that these environments elicit significant changes in assemblage structure, trophodynamics and carbon cycles. Chemosynthetic activity generally did not constitute a major proportion of the diet of any assemblage, even at the most hydrothermally active sites, but was detected in macrofaunal food webs at very surprising distances (~ 100km) from the (known) sites of active venting. This research illustrates and examines the impacts that these environments can have upon a range of ecological processes and raises questions about the full extent and significance of chemosynthetic organic matter production in seafloor ecosystems.
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